Detection of hydrodynamic stimuli by the Florida manatee (Trichechus manatus latirostris)
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- Gaspard, J.C., Bauer, G.B., Reep, R.L. et al. J Comp Physiol A (2013) 199: 441. doi:10.1007/s00359-013-0822-x
Florida manatees inhabit the coastal and inland waters of the peninsular state. They have little difficulty navigating the turbid waterways, which often contain obstacles that they must circumnavigate. Anatomical and behavioral research suggests that the vibrissae and associated follicle–sinus complexes that manatees possess over their entire body form a sensory array system for detecting hydrodynamic stimuli analogous to the lateral line system of fish. This is consistent with data highlighting that manatees are tactile specialists, evidenced by their specialized facial morphology and use of their vibrissae during feeding and active investigation/manipulation of objects. Two Florida manatees were tested in a go/no-go procedure using a staircase method to assess their ability to detect low-frequency water movement. Hydrodynamic vibrations were created by a sinusoidally oscillating sphere that generated a dipole field at frequencies from 5 to 150 Hz, which are below the apparent functional hearing limit of the manatee. The manatees detected particle displacement of less than 1 μm for frequencies of 15–150 Hz and of less than a nanometer at 150 Hz. Restricting the facial vibrissae with various size mesh openings indicated that the specialized sensory hairs played an important role in the manatee’s exquisite tactile sensitivity.
Minimum angle of resolution
Manatees possess a unique arrangement of specialized sensory hairs, classified as vibrissae, present on the face and across the body. Anatomical and neurophysiological evidence in conjunction with behavioral assessments from other species as well as manatees suggest that vibrissae play an important role in detecting environmental stimuli.
Each vibrissal apparatus is known as a follicle–sinus complex (FSC), which includes a blood-filled sinus, bounded by a dense connective tissue capsule, is robustly innervated, and provides haptic feedback to the animal (Dykes 1975; Rice et al. 1986). Vibrissae are located primarily on the mystacial region of terrestrial and non-sirenian aquatic mammals, and are commonly referred to as whiskers. They can possess a number of mechanoreceptors such as Merkel cells, lanceolate endings, and free nerve endings (Zelena 1994). A deep vibrissal nerve containing 100–200 axons is found in rodents (Rice et al. 1986), whereas a number of aquatic mammals possess several main nerves, and a higher number of axons per follicle (Dehnhardt et al. 1999; Reep et al. 2001; Sarko et al. 2007). Ringed seals have between 1,000 and 1,500 axons per vibrissa (Hyvärinen 1995) and bearded seals exhibit a similar range, with a maximum of 1,650 (Marshall et al. 2006). The Australian water rat, which lives on land but hunts for prey in water, displays a count of 500 axons per follicle, intermediate between terrestrial and aquatic species (Dehnhardt et al. 1999). Manatees have up to 250 axons per FSC of the facial region (Reep et al. 2001).
Aquatic mammals face a unique challenge that terrestrial mammals do not. The increased density of water in comparison with air causes a constant deflection of vibrissae during any movement. Hanke et al. (2010) noted that harbor seals possess vibrissae that have an undulated surface structure. This specialization results in reduced vibrissal vibration, and thus a reduction in self-noise during swimming. The efference copy mechanism that has been documented in some fishes (Bell 1982; Coombs et al. 2002), allowing the organism to differentiate between externally generated stimuli versus those resulting from its own actions, could also be utilized by aquatic mammals.
To obtain information about their environment, aquatic mammals have developed adaptations of vibrissal systems. Walruses use their stiff vibrissae to explore the benthic substrate in search of invertebrates and are able to discriminate different objects at a small scale (Fay 1982; Kastelein and van Gaalen 1988). Seals and sea lions have been found to discriminate fine differences in objects (Dehnhardt 1994; Dehnhardt and Kaminski 1995; Dehnhardt and Dücker 1996). Seals can detect low-frequency hydrodynamic stimuli (Dehnhardt et al. 1998), and sea lions (Gläser et al., 2011) as well as seals (Dehnhardt et al. 2001; Schulte-Pelkum et al. 2007) can follow hydrodynamic trails generated by swimming conspecifics or as might be generated by prey. Manatees use their facial vibrissae to investigate food items and novel objects (Hartman 1979; Marshall et al. 1998; Bachteler and Dehnhardt 1999; Reep et al. 2002). They may also use them to detect hydrodynamic stimuli.
Manatees have only vibrissae and no other hair type distributed over their bodies. This arrangement appears to be unique among mammals, although rock hyraxes, a terrestrial relative of manatees, have a similar distribution, but with the vibrissae intermixed with pelage (D. Sarko, pers. comm.). Vibrissae are ~30 times denser on the facial region than on the post-facial body. The lips of the manatee are very mobile and prehensile. The vibrissae on the upper lip (U2 field) and lower lip (L1 field) are everted during grasping of objects, including plants ingested during feeding. This oral grasping has been termed oripulation (Marshall et al. 1998; Reep et al. 1998). The number of axons per follicle decreases when traveling further from the oral cavity (Reep et al. 2001). Vibrissae on the oral disk, classified as bristle-like hairs (BLHs) that are intermediate in stiffness and innervation, are used in non-grasping investigation of objects and food items (Hartman 1979; Marshall et al. 1998).
A previous study with the same two Florida manatees used in the current research investigated their ability to perform active touch discrimination of texture gratings using the facial vibrissae. Weber fractions (just-noticeable-differences), the proportion change in size needed for the subject to detect a difference between objects, were measured and compared to those of other species. Both manatees demonstrated low Weber fractions. One subject was able to detect differences in size down to 0.025 of a standard with 2.0-mm gratings and the other subject down to 0.075 (Bauer et al. 2012). The present study sought to test the hypothesis that manatees use their facial vibrissae not only for active touch but also to detect hydrodynamic stimuli. We conducted three experiments to test this hypothesis. The first generated a manatee tactogram, tactile detection thresholds across a set of low frequencies. A second test restricted vibrissae to assess their involvement in detection of hydrodynamic stimuli. A third experiment assessed vibrissae sensitivity using a signal detection format.
Materials and methods
The subjects were two male Florida manatees (Trichechus manatus latirostris) housed at Mote Marine Laboratory and Aquarium in Sarasota, Florida, USA. Buffett and Hugh, 21 and 24 years of age, respectively, at the initiation of the study, had an extensive training history in the context of husbandry and sensory research (Colbert et al. 2001, 2009; Bauer et al. 2003; Mann et al. 2005; Bauer et al. 2012; Gaspard et al. 2012).
A dipole vibration shaker (Data Physics—Signal Force, Model V4, San Jose, CA, USA) with a 5.7-cm diameter rubberized sphere connected via a 35.6-cm, rigid, stainless steel extension rod was used to generate the stimuli. The dipole shaker generates a localized flow that decreases in amplitude as 1/distance3, as opposed to a monopole source that decreases in amplitude as 1/distance2 (Kalmijn 1988). To minimize any vibrational transfer between the shaker apparatus and the stationing apparatus, the stationing apparatus and the shaker mount were separated and buffered with shock absorbing foam.
The stimuli were generated digitally by a Tucker-Davis Technologies (TDT) Enhanced Real-Time Processor (RP2.1, Alachua, FL, USA; sample rate 24.4 kHz), attenuated with a TDT Programmable Attenuator (PA5) to control level, and amplified with a Samson Power Amplifier (Servo 120a, Hauppauge, NY, USA). The signal generating equipment was controlled by a program in MATLAB (The MathWorks, Natick, MA, USA) in conjunction with a graphical user interface (TDT Real-Time Processor Visual Design Studio) created specifically for this research. A digital output on an RP2.1 was used to control the LED that indicated the start of a trial. A separate D/A channel was used to generate the acoustic secondary reinforcer, which was presented through an underwater speaker (Clark Synthesis, Model AQ-39, Littleton, CO, USA) when the manatee was correct on a trial. The speaker was located >1 m away from the subject and also presented noise (151 dB re 1 μPa; 0–12.2 kHz bandwidth) constantly through the session to mask any auditory artifacts from the generation of the hydrodynamic stimulus. These signals were amplified by a separate amplifier (American Audio, Model VLP 300, Los Angeles, CA, USA) to avoid crosstalk.
For stimuli analysis and calibration, a 3-dimensional accelerometer (Dimension Engineering, Model DE-ACCM3D, Akron, OH, USA) was embedded into the sphere to measure its movement. MATLAB was used to calculate, plot, and log the stimulus for each trial. This accelerometer was used to monitor the shaker operation during testing. To calculate particle motion from the dipole for threshold measurements, a 3-D accelerometer was mounted to a neutrally buoyant, spring-mounted geophone. The outputs from all three channels were recorded simultaneously by the RP2.1. The rms acceleration of the unattenuated stimulus for each stimulus frequency was calculated from these recordings. The magnitude of acceleration from all three axes was calculated as the square root of the sum of squares of each axis. The acceleration at the threshold was calculated by scaling the acceleration measured at no attenuation by the attenuation at threshold. For sinusoidal signals, particle velocity is the particle acceleration divided by 2πf, and particle displacement is particle velocity divided by 2πf (where f = frequency in Hertz). The sensitivity of the accelerometer was verified by comparing its output when directly vibrated with the output of a laser vibrometer (Polytec, Model CLV 1000, Irvine, CA, USA) pointed at the accelerometer. The laser vibrometer could not be used in the manatee tank because it only measures motion in one direction along the laser beam.
To ensure that the test subjects were not cued during testing, a number of protocols and measurements were conducted. A 3-D accelerometer was routinely attached to the stationing apparatus to ensure that there was no vibrational transfer from the shaker during presentation trials. The subjects’ minimum angle of visual resolution (MAR) [(Buffett’s MAR = 21 arc minutes and Hugh’s MAR = 66 arc minutes (Bauer et al. 2003)] precluded detection of the maximum sphere movement at threshold (0.0095 cm), which subtended a visual angle of less than 0.02 arc minutes for each manatee. The research trainer responsible for verifying the position of the manatee and providing the primary reinforcement was blind to whether the ensuing trial was a stimulus-present or stimulus-absent trial. This trainer was also out of sight of the manatee and remained motionless until the trial sequence was complete.
Experiment I: Tactogram
The tactogram established the tactile thresholds for frequencies ranging from 5 to 150 Hz. The upper limit was selected to minimize the possibility that detection of the stimuli by hearing confounded tactile measurements.
Experiment II: Restriction Tests
Hole size of mesh netting and the approximate percentage of facial vibrissae that were restricted
Mesh hole size (mm)
Vibrissae restricted (%)
35 μm (0.035)
Experiment III: Signal Detection Tests
Threshold measures are influenced by decision criteria. An alternative way to address sensitivity while controlling for these criteria is to use a signal detection analysis (Gescheider 1997). Detection testing was conducted under two conditions, with and without the fine mesh (0.397 mm), at 25 Hz at 0.21 μm displacement, a 3.35× (10.5 dB) attenuation from the starting level during threshold testing. Fifty trials were conducted under each condition (25 signal present; 25 signal absent). Values for d’ and C were calculated. In signal detection theory d’ is an unbiased sensitivity parameter. C is an index of the decision criterion. Unbiased responses are indicated by C values approaching zero. Values of C < 0 indicate a greater probability of reporting a signal present when it is not, a false alarm, and values >0 indicate a greater probability of reporting a signal absent when it is in fact present (Gescheider 1997).
Experiment I: Tactogram
Facial threshold values and false alarm rate for each tested frequency for Buffett and Hugh
False alarm rate
Experiment II: Restriction Trials
Displacement thresholds (μm) for each frequency (Hz) based on mesh size
35 μm mesh
Experiment III: Signal Detection
Signal detection theory analysis of testing under no mesh and fine mesh conditions for Buffett
The thresholds determined for the facial vibrissae of manatees demonstrate remarkable sensitivity, highlighted by the detection of particle displacement approaching and below 1 nm at 150 Hz. Dehnhardt et al. (1998), in a study which served as a model for this one, tested the ability of a harbor seal (Phoca vitulina) to detect hydrodynamic stimuli. Comparing the data, the manatees were more sensitive by an order of magnitude (Fig. 4) and more recent research has established that the California sea lion (Zalophus californianus) has an intermediate sensitivity (Dehnhardt and Mauck 2008). Manatees often inhabit bodies of water with very little water motion, and this high sensitivity may allow them to sense their environment through detection of boundary layers, in-water obstacles, and changes in water currents. Signals with a high frequency could be related to the manatee swimming through a boundary, but also could be related to movement of vibrissae during normal swimming, and provide an indication of swimming speed.
Comparing the thresholds as a function of displacement, velocity, or acceleration shows a much larger range for displacement than velocity or acceleration. We do not know which modality or modalities the vibrissae sense. Studies with rat whiskers suggest that they are velocity-sensitive because thresholds varied as a function of stimulus amplitude or frequency, but not as a function of amplitude × frequency (Adibi et al. 2012).
As a greater percentage of the vibrissae were limited, the manatees’ thresholds increased and the subjects were not able to detect the stimuli at the lower frequencies when they were completely restricted. These results strongly suggest that tactile senses, including those mediated by the vibrissae, were responsible for the observed thresholds, and not some other sense such as vision or hearing. MARs for both animals (Bauer et al. 2003) were above the angle of resolution necessary to see the distance moved by the stimulus sphere displacement. Auditory thresholds of manatees are highest at low frequencies (Gerstein et al. 1999; Gaspard et al. 2012). Note that one of the two manatees tested by Gerstein (1999) could detect the acoustic signals from 15 to 400 Hz with thresholds from 93 to 111 dB re 1 μPa. However, Gerstein et al. (1999) suggested that under 400 Hz the manatee was detecting the stimulus tactually, rather than by hearing, based on response characteristics.
In the restriction experiments, there was convergence of sensitivity at the higher frequencies as it appeared that the mesh had less effect at these frequencies. The mechanism of detection may change at these frequencies, and could involve follicle-associated mechanoreceptors and surface Merkel cells. The increase of thresholds during restriction testing and the decrease in d’ with the inclusion of the mesh netting during signal detection tests indicates that the vibrissae were a key component to the detection of low-frequency vibratory stimuli.
It is not known what cues manatees use for orientation as they navigate through their environment and migrate between summer and winter refugia. They spend a significant portion of time in turbid waters, especially during travel, but they have poor visual acuity (Mass et al. 1997, 2012; Bauer et al. 2003) and do not echolocate. Previous work has shown that the perioral bristles play a dominant role during feeding and oripulation (Hartman 1979; Marshall et al. 1998; Bachteler and Dehnhardt 1999; Bauer et al. 2012). The BLHs of the oral disk may serve as a sensory array to detect hydrodynamic stimuli, in addition to their use in direct contact tactile scanning (Bauer et al. 2012). The anatomical differentiation between the stout perioral bristles and the more pliant BLHs supports the likelihood of a role for the latter in passive detection of hydrodynamic stimuli (Sarko et al. 2007). Furthermore, our failure to observe the subjects flare their lips to expose the perioral bristles during exposure to the vibratory stimuli suggests that they do not play a role in passive detection, leaving the BLHs as the most likely vibrissae to be involved in facial sensitivity to hydrodynamic flow.
Bearded seals and ringed seals possess FSCs innervated by more than 1,000 axons per vibrissa (Hyvärinen 1995; Marshall et al. 2006) with rodents demonstrating significantly less innervation at 100–200 per FSC (Rice et al. 1986). The Australian water rat, since it does not live exclusively in an aquatic environment, and displays an intermediate number of axons per follicle (~500), seems to optimize its existence in both mediums (Dehnhardt et al. 1999). The increased innervation of aquatic species highlights the specialization required to exist in a complex environment. The facial region of the manatee is densely populated with approximately 2,000 vibrissae with over 100,000 associated axons innervating these FSCs and approximately 600 are the BLHs located on the oral disk (Reep et al. 1998; 2001). This axonal innervation, up to 250 axons per facial vibrissae, is comparable to the specialized nasal region of the star nosed mole (Catania and Kaas 1997).
The FSCs of manatees possess Merkel endings that are found within the ring sinus and at the rete ridge collar in post-facial and bristle-like hairs (BLHs) which may allow for the extraction of multiple features of a stimulus, potentially including the intensity, direction, velocity, and acceleration of hair deflection (Rice et al. 1997; Ebara et al. 2002; Sarko et al. 2007). Merkel cells in the post-facial FSCs are highly innervated in contrast to the facial vibrissae (Sarko et al. 2007), possibly implicating the facial vibrissae in “active” touch and the post-facial FSCs in a “passive” detection system. Sarko et al. (2007) discovered a “tangle” nerve ending unique to manatees that might act as a low threshold mechanoreceptor, indicating a possible increase in sensitivity of manatees to minute stimuli. Vibrissae on non-mystacial regions have been demonstrated to play a crucial role in some species. Naked mole rats use modified hairs located on their bodies for orientation and some squirrels and jerboas possess tactile hairs on their extremities that could provide feedback about landing sites after jumps (Sokolov and Kulikov 1987; Crish et al. 2003). These peripheral specializations of the manatee somatosensory system are supported by larger regions of the somatosensory brainstem, thalamus, and cortical regions featuring specialized neuronal aggregations (Rindenkerne) which are analogous to the barrel cortex in rodents (Reep et al. 1989; Marshall and Reep 1995).
Behavioral studies with mottled sculpin (Cottus bairdi) using a dipole found acceleration thresholds of about 0.18 mm/s2 for 10–100 Hz (Coombs and Janssen 1989a, b, 1990). This is about 4–20 times more sensitive than the manatee facial vibrissae thresholds over the same frequency range. Several studies have investigated the ability of fish to detect particle displacement; however, these were primarily measured in primary auditory afferents, perceived as acoustic stimuli. Oscars (Astronotus ocellatus) detected article displacement of 1.2–1.6 nm (RMS) at 100 Hz (Lu et al. 1996). Similar sensitivity was demonstrated by goldfish (Carassius auratus) and toadfish (Opsanus tau) with a detection of particle displacement less than 1 nm (RMS) (Fay and Olsho 1979; Fay 1984; Fay et al. 1994). Particle displacement sensitivity for the manatees at 100 Hz was 1.9 and 3.1 nm (Table 2). Although the detection modality sometimes differed in fish, the manatees were able to detect the particle displacement at slightly higher levels.
Blind cavefish sense objects in the water by detecting alterations in self-produced hydrodynamic stimuli as they go near or pass them (von Campenhausen et al. 1981; Weissert and von Campenhausen 1981; Hassan 1989). Future research should investigate whether manatees utilize their own self-generated hydrodynamic stimuli in a similar manner to the blind cave fish, which detect reflected bow waves or interruptions of the pressure waves, gaining information about their typically turbid environment. The vibrissae of manatees are anatomically specialized and behaviorally utilized to detect hydrodynamic stimuli, supporting and strengthening the hypothesis that the vibrissae act as a sensory array analogous to the lateral line system of fish.
The authors would like to thank the United States Fish and Wildlife Service (Permit MA837923-6/7); the Florida Fish and Wildlife Conservation Commission; University of Florida, College of Veterinary Medicine—Aquatic Animal Health Program; Mote Marine Laboratory staff, interns, volunteers, especially trainer Jann Warfield, that assisted with this research; Guido Dehnhardt and Wolf Hanke for their expertise and equipment loan during training; Ronnie and John Enander; the Thurell family; New College of Florida students; Peg Scripps Buzzelli Chair, New College Foundation. This work was supported by the National Science Foundation (IOS-0920022/0919975/0920117). All experimental procedures were approved by the Mote Marine Laboratory IACUC prior to implementation.